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Microcystic Inner Nuclear Layer Abnormalities and Neuromyelitis Optica

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Microcystic Inner Nuclear Layer Abnormalities and Neuromyelitis Optica ORIGINAL CONTRIBUTION Microcystic Inner Nuclear Layer Abnormalities and Neuromyelitis Optica Jeffrey M. Gelfand, MD; Bruce A. Cree, MD, PhD, MRC; Rachel Nolan, BA; Sam Arnow, BS; Ari J. Green, MD, MCR Importance: Microcystic abnormalities involving the in- function. The hypothesis was generated prior to the data ner nuclear layer of the retina occurs in a subset of pa- being reviewed and analyzed. tients with multiple sclerosis, most commonly in eyes pre- viously affected by symptomatic optic neuritis. Acute optic Results: Microcystic changes were identified in 5 of 25 neuritis is a cardinal manifestation of neuromyelitis op- patients with NMO (20%) and 7 of 48 total eyes, includ- tica (NMO). To our knowledge, microcystic inner nuclear ing 7 of 29 eyes (24%) previously affected by optic neu- layer abnormalities have not been investigated in NMO. ritis. Microcystic changes occurred exclusively in eyes with a history of acute symptomatic optic neuritis (100% Objective: To establish whether microcystic inner of eyes with microcystic changes had experienced prior nuclear layer abnormalities occur in NMO. optic neuritis compared with 71% of NMO eyes without microcystic abnormalities). There were no significant dif- Design: Observational, retrospective study. ferences between patients with NMO with and without microcystic changes in terms of age, sex, and aquaporin Setting: University of California at San Francisco Mul- 4–IgG antibody status. The mean age in this cohort was tiple Sclerosis Center (academic specialty clinic). 44 years (range, 13-81 years); 84% were women; 80% were aquaporin 4–IgG seropositive; and the median Ex- Patients: Twenty-five consecutive patients with NMO based on 2006 diagnostic criteria or with NMO spec- panded Disability Status Scale score was 4.0 (interquar- trum disease (defined by seropositivity for anti– tile range, 3.0-6.5). aquaporin 4 IgG in the context of a single episode of trans- verse myelitis or optic neuritis). Conclusions and Relevance: Microcystic inner nuclear layer pathology occurs in a proportion of patients with Exposure: Spectral-domain optical coherence tomog- NMO in eyes previously affected by acute optic neuritis. raphy. Additional research is needed to understand the cause of this retinal pathology and determine whether it con- Main Outcomes and Measures: Identification of mi- tributes to persistent visual disability in patients with NMO crocystic inner nuclear layer pathology on spectral- following optic neuritis. domain optical coherence tomography. Multivariable lin- ear regression was used to examine associations between JAMA Neurol. 2013;70(5):629-633. Published online microcystic changes and measures of retinal structure and March 25, 2013. doi:10.1001/jamaneurol.2013.1832 EUROMYELITISOPTICA Optic neuritis is a defining feature of (NMO) is an inflamma- NMO and typically leads to optic nerve de- tory disease of the cen- myelination,11 profound retinal nerve fi- tral nervous system char- ber layer (RNFL) axonal loss,12-16 retinal acterized by injury to the ganglion cell loss,17 and severe visual dis- optic nerve, spinal cord, brainstem, and ability.18-20 Optic neuropathy in NMO is N 1,2 brain parenchyma. Once thought to be also sometimes associated with peripap- an aggressive variant of multiple sclero- illary retinal vascular abnormalities, in- sis (MS), NMO is now known to have a cluding focal arteriolar narrowing and at- Author Affiliations: Multiple distinctive pathophysiology character- tenuation of the peripapillary vascular Author Aff Sclerosis Center, Department of ized, in part, by an antibody-mediated tree.15 Sclerosis Ce Neurology (Drs Gelfand, Cree, attack against central nervous system aqua- Microcystic macular edema, a novel Neurology and Green, Ms Nolan, and porin 4,3-5 a water channel expressed by retinal phenotype characterized by hon- and Green, Mr Arnow) and Department of 6-8 Mr Arnow) Ophthalmology, astrocytes. Serum IgG-1 antibodies to eycombed, microcystic abnormalities of Ophthalmo Neuro-Ophthalmology Service aquaporin 4 are detectable in about 80% the inner nuclear layer on optical coher- Neuro-Oph (Dr Green), University of of patients with NMO and are highly spe- ence tomography (OCT), was recently (Dr Green) California, San Francisco. cific for the diagnosis.3,9,10 identified and confirmed to occur in about California, JAMA NEUROL/ VOL 70 (NO. 5), MAY 2013 WWW.JAMANEURO.COM 629 ©2013 American Medical Association. All rights reserved. Downloaded From: http://archneur.jamanetwork.com/ by a University of California - San Francisco User on 11/05/2013 5% of patients with MS.21,22 Microcystic inner nuclear layer to read at 20/200). Color vision was tested using Hardy-Rand- abnormalities have also been observed histologically fol- Rittler color plates.32 lowing optic nerve transection23-25 and as rare findings in other types of human optic nerve injury,26 but this find- STATISTICAL ANALYSIS ing has not been consistently replicated in other model systems of optic nerve injury.27,28 Multivariable linear regression was used to examine associa- In this study, we sought to establish whether micro- tionsofmicrocysticinnernuclearlayerpathologywithfovealthick- cystic inner nuclear layer pathology occurs in NMO. ness, macular volume, RNFL thickness, visual acuity, and EDSS, with models adjusting for age and sex and, when appropriate, his- tory of optic neuritis. Within-patient intereye correlations were METHODS accounted for using the robust clustered sandwich estimator. Dif- ferences in baseline variables between groups were analyzed using PARTICIPANTS the t test for age, the ␹2 test for sex, the Fisher exact test for optic neuritis, and the Wilcoxon rank-sum test for EDSS and time from We retrospectively identified consecutive patients with NMO first and most recent acute optic neuritis. Stata version 12.0 (Stata- based on 2006 diagnostic criteria29 or with NMO spectrum dis- Corp) was used for all analyses. ease (defined by seropositivity for anti–aquaporin 4 IgG in the context of a single episode of transverse myelitis or optic neu- RESULTS ritis) who had received spectral-domain (SD)–OCT imaging at our referral center as part of routine clinical care between 2008 and 2012. Exclusion criteria included diabetes mellitus, glau- We identified 23 patients with NMO and 2 patients with coma, uveitis, eye trauma, or other retinal disease. A history of acute optic neuritis was defined clinically and was obtained by NMO spectrum disorder (both with optic neuritis and participant report and medical record review. The Expanded positive anti–aquaporin 4 IgG) who had received SD- Disability Status Scale (EDSS) score,30 a measure of functional OCT imaging in our laboratory as part of routine clini- disability typically used in MS but also potentially informative cal care between 2008 and 2012. The mean (SD) age of in NMO, was assigned by the treating neurologist. Aquaporin this cohort was 44.2 (18.5) years (range, 13-81 years); 4 antibody testing was obtained from one of several commer- 84% were women; 15 (60%) were white (of whom 2 were cial laboratories. of Hispanic ethnicity), 7 (28%) were Asian, and 3 (12%) were black; 80% were aquaporin 4–IgG seropositive; and ETHICAL CONSIDERATIONS the median EDSS score was 4.0 (interquartile range, 3.0- 6.5). Two eyes were excluded from analysis owing to dif- All patients provided written informed consent. The Univer- ficulty obtaining interpretable scans in the context of se- sity of California at San Francisco Committee on Human Re- vere visual loss. search approved the study protocol. Microcystic inner nuclear layer pathology was iden- tified on SD-OCT in 5 patients (20%) and in 7 of 48 eyes OCT (15%), including 7 of 29 eyes (24%) previously affected Spectral-domain OCT imaging was obtained using the Heidel- by optic neuritis (Table; Figure; eFigure, http://www berg Spectralis OCT system. For evaluation of the macula, we .jamaneuro.com). When compared with patients with MS used raster scans of the macula (20Њϫ15Њ) consisting of 19 line who underwent this identical diagnostic analysis at our scans in a rectangular section. A 360Њ peripapillary RNFL B- institution,21 microcystic changes were more common in scan was obtained at a distance of 3.4 mm from the center of patients with NMO (20%, 5 of 25) in our data set than the papilla and mean RNFL thickness was calculated using in those with MS (5%, 15 of 318) (P=.01; Fisher exact Heidelberg software.31 Laboratory-quality control measures in- test). Microcystic abnormalities occurred exclusively in cluded review of all source images to ensure adequate signal eyes previously affected by acute optic neuritis (100% of to noise, a good fit, and the absence of other significant retinal eyes with microcystic changes had prior optic neuritis or optic nerve pathology. Our laboratory target for macular scans compared with 71% of NMO eyes without microcystic was an automatic real-time (the number of B-scan images used to construct the final A-scan image) of 48 and a quality score changes; P=.17). The median time from the first optic (a measure of signal to noise) of 20. A trained technician ob- neuritis episode in the group with microcystic changes tained all OCTs. Microcystic inner nuclear layer abnormali- was 6.4 years (interquartile range, 5.6-10.2 years) com- ties were defined as cystic, honeycombed, lacunar areas of hy- pared with 4.5 years (interquartile range, 0.4-8.6 years) poreflectivity with clear boundaries on SD-OCT macular raster in NMO optic neuritis eyes without microcystic changes scan images, excluding speckling artifact.21 (P=.16). There were no appreciable differences in age, sex, aquaporin 4 antibody seropositivity, or EDSS score VISUAL TESTING between patients with and without microcystic changes. High-contrast and low-contrast vision and color vi- High-contrast visual acuity was measured using a computer- sion trended lower in eyes with microcystic changes, but ized Early Treatment Diabetic Retinopathy Study chart this difference did not reach statistical significance. The (ProVideo) under standard lighting conditions in the same ex- total RNFL was thinner in eyes with microcystic changes amination room using a standardized laboratory protocol.
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